Interpretive Summary: The potato late blight pathogen, Phytophthora infestans, is able to rapidly evolve to overcome resistance genes. The pathogen accomplishes this by secreting an arsenal of proteins, termed effectors, that function to modify host cells. Although hundreds of candidate effectors have been identified in P. infestans, their roles in pathogenicity or virulence remains basically unknown. Our results showed that one of these effectors functions to turn off resistance mediated by the potato gene RB. This effector accomplishes this by directly interacting with RB, which likely modifies its ability to turn on host resistance. Further molecular analysis identified two amino acids within the effector that determine interaction, which will assist in developing appropriate disease control strategies. Since this is the first example of an oomycete effector suppressing a host R protein, these results have advanced our basic knowledge of the function of pervasive oomycete effectors. This work has also impacted potato breeding and selection of disease resistant germplasm through the identification of RB-like genes that can resist effector suppression.

Technical Abstract:
Despite intensive breeding efforts, potato late blight, caused by the oomycete pathogen Phytophthora infestans, remains a threat to potato production worldwide because newly evolved pathogen strains have overcome major resistance genes. The Rpi-blb1 gene (also known as RB), from the wild potato Solanum bulbocastanum, confers resistance to most P. infestans strains through recognition of members of the pathogen effector family IPI-O. While the majority of IPI-O proteins are recognized by Rpi-blb1 to elicit resistance (e.g. IPI-O1, IPI-O2), some family members are able to elude detection (e.g. IPI-O4). In addition, IPI-O4 blocks recognition of IPI-O1, leading to inactivation of Rpi-blb1-mediated programmed cell death in Nicotiana benthamiana. Our results indicate a physical interaction between the Rpi-blb1 coiled coil (CC) domain and IPI-O4, but not with IPI-O1 as well as self-association of the Rpi-blb1 CC domain. We have identified four amino acids within IPI-O4 that are critical for interaction with the Rpi-blb1 CC domain. One of the amino acids, at position 129, also determines hypersensitive response induction. IPI-O1 mutant L129P fails to induce HR in presence of Rpi-blb1, however, IPI-O4 mutant P129L gains the ability to induce an HR. IPI-O1 L129P is also able to suppress the HR mediated by Rpi-blb1, indicating a critical step in the evolution of this gene family. Our results point to a model in which IPI-O4 can affect Rpi-blb1 function through its interaction with the Rpi-blb1 CC domain, possibly by preventing Rpi-blb1 dimerization or polymerization.